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Evolution in a Clade of Specialized Plant-Feeding Insects Evidence That Downloaded from rspb.royalsocietypublishing.org on March 2, 2010 Evidence that female preferences have shaped male signal evolution in a clade of specialized plant-feeding insects Rafael L Rodríguez, Karthik Ramaswamy and Reginald B Cocroft Proc. R. Soc. B 2006 273, 2585-2593 doi: 10.1098/rspb.2006.3635 References This article cites 43 articles, 5 of which can be accessed free http://rspb.royalsocietypublishing.org/content/273/1601/2585.full.html#ref-list-1 Receive free email alerts when new articles cite this article - sign up in the box at the top Email alerting service right-hand corner of the article or click here To subscribe to Proc. R. Soc. B go to: http://rspb.royalsocietypublishing.org/subscriptions This journal is © 2006 The Royal Society Downloaded from rspb.royalsocietypublishing.org on March 2, 2010 Proc. R. Soc. B (2006) 273, 2585–2593 doi:10.1098/rspb.2006.3635 Published online 1 August 2006 Evidence that female preferences have shaped male signal evolution in a clade of specialized plant-feeding insects Rafael L. Rodrı´guez*, Karthik Ramaswamy and Reginald B. Cocroft 223 Tucker Hall, Biological Sciences, University of Missouri–Columbia, Columbia, MO 65211-7400, USA Mate choice is considered an important influence in the evolution of mating signals and other sexual traits, and—since divergence in sexual traits causes reproductive isolation—it can be an agent of population divergence. The importance of mate choice in signal evolution can be evaluated by comparing male signal traits with female preference functions, taking into account the shape and strength of preferences. Specifically, when preferences are closed (favouring intermediate values), there should be a correlation between the preferred values and the trait means, and stronger preferences should be associated with greater preference–signal correspondence and lower signal variability. When preferences are open (favouring extreme values), signal traits are not only expected to be more variable, but should also be shifted towards the preferred values. We tested the role of female preferences in signal evolution in the Enchenopa binotata species complex of treehoppers, a clade of plant-feeding insects hypothesized to have speciated in sympatry. We found the expected relationship between signals and preferences, implicating mate choice as an agent of signal evolution. Because differences in sexual communication systems lead to reproductive isolation, the factors that promote divergence in female preferences—and, consequently, in male signals—may have an important role in the process of speciation. Keywords: vibrational signalling; sexual coevolution; phytophagous insects; Hemiptera; Membracidae 1. INTRODUCTION influence the variability of signal traits; (iv) when Mate choice is widespread in nature and regarded as comparing closed preferences with open preferences, a strong and pervasive influence in the evolution of which favour values in one extreme of the range, the mating signals and other sexual traits (Darwin 1871; former will be associated with lower signal variability West-Eberhard 1983; Andersson 1994). The importance (Gerhardt 1994; Shaw & Herlihy 2000; Gerhardt & Huber of mate choice in signal evolution can be evaluated by 2002); and (v) for open preferences that differ in strength comparing signal traits with mate preferences. Prefer- or sign, signal traits should be shifted towards the ences can be described using curves that plot attractive- preferred values (Houde & Endler 1990; Endler & ness as a function of variation in signal traits, and Houde 1995; Simmons et al. 2001). characterizing preference functions generates hypotheses We evaluated the importance of female mate choice in about the type of selection they exert on signals (Butlin signal evolution by testing these predictions across four 1993; Gerhardt 1994; Ritchie 1996; Jang & Greenfield species in the Enchenopa binotata species complex of 1998; Gerhardt et al. 2000; Shaw & Herlihy 2000; treehoppers. This complex consists of 11 or more species Ritchie et al. 2001; Parri et al. 2002; Blows et al. 2003; that occur in close sympatry across eastern North America, and differ in male mating signals. In the mating system Klappert & Reinhold 2003; Brooks et al. 2005; Gerhardt of these insects, male–female duetting facilitates pair 2005a,b; Bentsen et al. 2006). Comparison of prefer- formation, so female response signals provide an assay of ences with the distribution of signal traits for closely mate preference (Rodrı´guez et al. 2004). We found that related species or populations can reveal the extent to preferences differ among species in the E. binotata which signals have responded to selection exerted complex, and that signals match the values preferred by by preferences. the females to a degree that is determined by preference The hypothesis that mate choice is important in signal strength and shape. evolution makes five predictions about the preference– signal relationship: (i) for closed preferences—which favour intermediate over extreme values—mean signal values will correspond to the values preferred by females 2. MATERIAL AND METHODS (Ritchie 1996; Shaw 2000; Mendelson & Shaw 2002; (a) The Enchenopa binotata species complex Gerhardt 2005a,b); (ii) preference strength will influence (Hemiptera: Membracidae) the degree of correspondence between preferred values Each species in this clade specializes on a different species of woody plant in the forest understory, edge and canopy. The and mean signal traits; (iii) preference strength will E. binotata complex is a case study of sympatric speciation involving shifts to novel host plants (Wood & Guttman 1983; * Author for correspondence ([email protected]). Wood & Keese 1990; Wood et al. 1990; Lin & Wood 2002; Received 21 April 2006 2585 q 2006 The Royal Society Accepted 29 May 2006 Downloaded from rspb.royalsocietypublishing.org on March 2, 2010 2586 R. L. Rodrı´guez and others Female preferences and signal evolution (a) included dominant frequency at the end of the whine, whine length, number of signals per bout, length of the interval 1000 between signals, pulse number and pulse rate (figure 1). We varied one trait at a time while keeping the other traits set to the mean of the local population from which females were drawn. The values assayed for each trait span the range of frequency (Hz) frequency 200 variation in the complex. For signal frequency, this range 200 ms (100–500 Hz) did not reach frequencies high enough to describe the full shape of the E. binotata ‘Celastrus’ preference, so we extended the range of frequencies to whine pulses 720 Hz for two additional females. (b) Rather than relying on natural variation in mating signals, we synthesized signals with a custom-written program in MATLAB v. 5.2.1 (Mathworks Inc., Natick, 1 s MA). Preliminary experiments showed that these signals are as effective in eliciting female responses as Figure 1. (a) Spectrogram and waveform of a recording of a playbacks of recorded male signals (R. L. Rodrı´guez 2006, signal produced by a male E. binotata ‘Viburnum’. (b) Bout consisting of four signals that increase in amplitude. unpublished data). The artificially generated signals use a constant frequency rather than a frequency sweep; this Cocroft et al. in press). Host shifts cause assortative mating, greatly streamlines the playback procedure, as they do not because the insects’ life-history timing is regulated by host require compensation for differential frequency filtering plant phenology, so insects on plants with different phenol- during propagation along plant substrates (Cocroft & ogies acquire allochronic life cycles. Host shifts also result in Rodrı´guez 2005). divergent ecological selection promoting host specialization Stimuli had the typical E. binotata signal bout structure and host fidelity. of gradually increasing amplitude (figure 1b). We used a Sexual communication is important for assortative mating structure of four signals that increased in amplitude in in this complex. As in many herbivorous insects (Claridge the pattern: 25, 75, 100 and 100% of maximum amplitude. 1985; Henry 1994; Cokl & Virant-Doberlet 2003; Cocroft & We varied this pattern only for the experiment testing the Rodrı´guez 2005), pair formation in E. binotata is facilitated signal number, where the one-signal stimulus had 100% by exchanges of plant-borne vibrational signals between amplitude and the two-signal stimulus had a pattern of 75 males and females (Hunt 1994; Sattman & Cocroft 2003; and 100% amplitude. Rodrı´guez et al. 2004). Mate-searching males produce signals, and female responses elicit localized searching by (d) Stimulation and recording of female responses the males. Signal structure is conserved across the complex, We played back stimuli to females through the stems of and consists of a tone with harmonics and a frequency sweep, potted plants (ca 50 cm tall) of their host species. To the whine, followed by a series of pulses (figure 1a). In spite introduce stimuli to a plant stem, we attached a magnet to of overall similarity in signal structure, there is quantitative the stem with wax (Endevco, San Juan Capistrano, CA) signal variation among species and individuals (R. B. Cocroft and placed an electromagnet ca 2mmfromit.The 2006, unpublished data). Females choose among males by electromagnet received signals from a Macintosh G4 responding to signals on the basis of this variation, computer, amplified with an Optimus MPA-40 amplifier. influencing the likelihood of being located by males Stimulus
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